Coral Reproduction on the World's Southernmost Reef at Lord Howe

Vol. 23: 275–284, 2015 AQUATIC BIOLOGY Published online April 13 doi: 10.3354/ab00627 Aquat Biol

OPENPEN ACCESSCCESS Coral reproduction on the world’s southernmost reef at Lord Howe Island, Australia

Andrew H. Baird1,*, Vivian R. Cumbo1, Sallyann Gudge2, Sally A. Keith1,3, Jeffrey A. Maynard4,5, Chun-Hong Tan1,6, Erika S. Woolsey1

1ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia 2NSW Department of Primary Industries, Lord Howe Island Marine Park, PO Box 161, Lord Howe Island, NSW 2898, Australia 3Center for Macroecology and Evolution, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark 4Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA 5Laboratoire d’Excellence «CORAIL» USR 3278 CNRS−EPHE, CRIOBE, Papetoai, Moorea, French Polynesia 6School of Marine Science and Environment, Universiti Malaysia Terengganu, 21030 Kuala Terengganu, Terengganu, Malaysia

ABSTRACT: Despite a recent expansion in the geographic extent of coral reproductive research, there remain many regions in the Indo-Pacific where knowledge is limited. For example, Lord Howe Island is the southernmost reef system in the world (31° S); however, very little is known of the reproductive biology of the coral fauna. Here, aspects of the reproductive biology and the timing of reproduction for 40 of the approximately 65 species that occur on Lord Howe Island are documented. In December 2010, field assessments of the stage of gamete maturity in Acropora spp. colonies suggested that 5 species spawned in December 2010 and 11 in January 2011. In January 2012, similar sampling suggested that 12 Acropora species spawned in January and 1 in February. In addition, 11 species from 10 genera broadcast spawned gametes from 17:30 to 24:00 h in January 2012, 10 to 12 d after full moon. Goniastrea favulus was inferred to spawn prior to 17:00 h, 6 to 12 d after full moon and Porites heronensis released brooded larvae. The reproductive biology of 3 other brooding species was examined using dissections and histology monthly for 1 yr from April 2011. Of these, Se- riatopora hystrix contained planulae between November 2011 and March 2012, Stylophora pistillata contained planulae between November 2011 and February 2012. No eggs or planulae were observed in Pocillopora damicornis. In conclusion, the spawning patterns on Lord Howe Island are consistent with other locations in the Indo-Pacific: multi-species synchronous spawning episodes occur after full moons, when water temperatures are relatively high.

KEY WORDS: Coral reefs · Larval ecology · Spawning timing · Egg size

INTRODUCTION often context-dependent suggests we should seek to quantify reproductive phenology across a wide geo- Coral reproductive research in the Indo-Pacific has graphic extent. Whilst the geographic focus of coral been concentrated historically in regions close to reproductive research has recently expanded to in - marine research stations in developed countries (see clude more remote regions such as India (Raj & review by Baird et al. 2009b). However, coral repro- Edward 2010), New Caledonia (Baird et al. 2010), the duction is increasingly recognised as a fundamental Persian Gulf (Bauman et al. 2011) and Yemen (Baird process to maintain ecosystem function within coral et al. 2014), reproductive phenology on marginal reefs and, as such, interest in improving our un- reefs at the extreme geographical limits of coral dis- derstanding of this process has grown rapidly. In tributions has yet to be quantified. Corals on mar- addition, recognition that ecological processes are ginal reefs would be expected to be the least con -

© The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 276 Aquat Biol 23: 275–284, 2015

sistent with a broader pattern and, therefore, offer 2009) and therefore replenishment is likely to be potential to determine the limits of reproductive highly dependent on local reproductive output or phenology. irregular input of propagules from distant upstream The increased geographical extent across which re- reefs (Fellegara et al. 2013, Madsen et al. 2014). productive phenology has been quantified has altered Most broadcast-spawning colonies spawn only once our understanding of coral reproductive synchrony per year (Harrison & Wallace 1990, Baird et al. 2009b). and the processes that regulate the timing of coral In contrast, oogenic cycles are much shorter in corals reproduction (Baird et al. 2009b, van Woesik 2010). that brood larvae (e.g. Stoddart & Black 1985, Per- For example, highly synchronous spawning, both mata et al. 2000), and consequently individual colonies within and among species, is not restricted to higher can release larvae multiple times per year. For exam- latitude reefs as earlier hypothesized (Oliver et al. ple, individual colonies of Pocillopora damicornis, 1988). In particular, multi-species synchronous spawn- Seriatopora hystrix and Stylophora pistillata release ing events (sensu Willis et al. 1985) are now de - larvae throughout the year at Palau, whereas at scribed for >25 locations globally (Baird et al. 2009b, Heron Island, on the southern Great Barrier Reef, Kongjandtre et al. 2010, Bouwmeester et al. 2011, breeding is seasonal (see review in Tanner 1996). Permata et al. 2012). In addition, coral reproduction Similarly, Isopora palifera releases planulae through- in most regions is highly seasonal, with the vast out the year in Papua New Guinea, but only in the majority of reproductive activity concentrated in 2 to summer months on Heron Island (Kojis 1986). 3 months each year (Baird et al. 2009a). This trend The highly seasonal nature of coral reproduction holds in equatorial locations (e.g. Singapore: Guest has important implications for reef ecology and con- et al. 2005; e.g. Kenya: Mangubhai & Harrison 2008) servation (Guest 2008). Numerous reef organisms, and in regions where breeding patterns had previ- including many fishes, time their reproductive cycles ously been described as aseasonal (e.g. the Red Sea: to benefit from this seasonal abundance of nutrients Shlesinger & Loya 1985) due to incomplete sampling (Pratchett et al. 2001, McCormick 2003). In addition, (Hanafy et al. 2010, Bouwmeester et al. 2015). knowledge of coral reef phenology allows the use of Despite this recent expansion in the geographic temporal management strategies that can mitigate extent of studies on coral reproduction, there remain the effects of coastal development on coral reefs many regions in the Indo-Pacific where research is (Richmond 1997). For example, dredging or discharge limited. For example, Lord Howe Island contains the of liquid waste from heavy industry can be prohibited southernmost reef system in the world (31.53° S, during coral spawning, ensuring that the seasonal 159.08° E); and is a World Heritage-listed marine pro- production of propagules for reef replenishment is tected area in the Tasman Sea, with highly distinc- not jeopardized (Baird et al. 2011). tive marine fauna including 9 endemic fish species In this study, we document the day or month of (Francis 1993) and 47 endemic species of algae (MPA propagule release for 34 of the approximately 65 coral 2010). Lord Howe Island supports a scleractinian species on Lord Howe Island. We also document fauna of approximately 65 species (Veron 1993); aspects of the reproductive biology of many of these however, almost nothing is known of the reproduc- species, including the sexual system, mode of larval tive biology of these corals, in particular the timing of development, transmission of Symbiodinium spp. and spawning and the length of the reproductive season. egg size on release. Goniastrea favulus was observed broadcast spawning at approximately 16:30 h ‘during mid-January, 1977’ (Kojis & Quinn 1981), 6 Acropora spp. and MATERIALS AND METHODS Cyphastrea microphthalma were observed setting (immediately prior to spawning) or spawning 8 to 9 Reproductive condition of Acropora species nights after the full moon, and Isopora cuneata plan- ulated 9 nights after the full moon in January 2007 Acropora were sampled 8 to 10 d before full moon (Harrison 2008). In addition, local tourist operators on 21 December 2010, and 3 to 5 d after full moon on often run nighttime snorkelling trips to observe 9 January 2012. These sampling times were chosen corals spawning following the full moon in February because previous work on Lord Howe Island indi- (P. Busteed pers. comm.). The reproductive bio logy cated that Acropora spp. spawn 8 to 10 d after full of high-latitude corals, such as those on Lord Howe moon (Harrison 2008). Twenty-three Acropora spp. Island, is of particular interest, because these popula- were sampled to determine their reproductive conditions are often geographically isolated (Noreen et al. tion (for full list of species see Table 1). Three repro- Baird et al.: Coral reproduction on Lord Howe Island 277

under the jetty during daylight hours (for species list see Table 2). Colonies were submerged in buckets and transported to the research station each day at 17:30 h, where they were maintained until 08:00 h the following morning, with 1 complete seawater change at 24:00 h. Colonies were inspected approximately ev ery 30 min while at the research sta tion to capture the onset of spawning. Egg colour, whether or not eggs were released in bundles, whether or not eggs contained Symbiodinium spp., and the maximum diameter of the spherical eggs were recorded. Egg size was measured to the nearest unit under a dissecting microscope with a stage micro meter and grati cule eyepiece at a magnification of ×40 from 2 to 6 h after egg release.

Reproductive biology of species in the family Pocilloporidae

To determine the reproductive condition of 3 species of pocilloporid corals (Pocillopora damicornis, Seriatopora hystrix, Stylophora pistillata), 1 branch, approximately 5 cm long, was collected from each of 5 colonies of each species monthly from April 2011 until March 2012 inclusive in the week before the full moon of each month. The fragments were preserved Fig. 1. Map showing the 4 collection sites at Lord Howe in 10% seawater formaldehyde and then decalcified Island: North Bay, Horseshoe, South Passage and Pot Holes. in a mixture of 90% water and 10% formic acid and All sites were within the lagoon, and the corals were collected 1 to 2 m below tidal datum. Mid-grey shadings are preserved in 70% ethanol. Five polyps were dis- areas of coral reef sected from each branch under a stereo-microscope and the numbers of oocytes and planulae in each polyp were counted. Oocytes and planulae of the ductive conditions were defined (sensu Baird et al. Pocilloporidae are readily distinguished under a 2002) based on the appearance of the oocytes stereo-microscope on the basis of size: oocytes rarely as observed with the naked eye in the field: (1) have a diameter >100 µm (Permata et al. 2000). The mature—oocytes pigmented and assumed to be type of reproductive tissue was confirmed through released within a month; (2) immature—oocytes pale histology. Sections of the decalcified branches con- but visible, indicating that they are close to maturity taining reproductive tissues were em bedded in wax and assumed to be released within 2 mo; and (3) following dissections, sectioned at 7 µm thickness, empty—oocytes too small to see or absent, indicating and 3 to 4 sections approximately 50 µm apart were either that the colony has recently released its mounted on slides. Slides were stained using Mayer’s gametes, or is unlikely to do so for at least 3 mo. haematoxylin and Young’s eosin-erythrosine (Baird et al. 2011).

Observations of coral reproductive behaviour in aquaria Environmental variables associated with coral spawning Mature coral colonies for spawning observations were collected from 1 to 2 m below tidal datum at 4 Environmental variables hypothesized to serve as sites (North Bay, Pot Holes, Comet’s Hole, South Pas- proximate cues by which coral synchronise spawning sage) in the lagoon on Lord Howe Island (Fig. 1) (see review in Baird et al. 2009b) were collated and between 16 and 20 January 2011 and were stored their association with the timing of spawning on Lord 278 Aquat Biol 23: 275–284, 2015

Howe Island illustrated graphically. Table 1. The reproductive condition of 23 Acropora spp. on Lord Howe Island This included monthly mean sea- in December 2010 and January 2012. Values represent percentage of colonies in each category. Imm.: immature; n: number of colonies sampled surface temperatures (SST), photo- synthetically available radiation (PAR), rainfall and wind speeds. Mean SSTs Species December 2010 January 2012 Mature Imm. Empty n Mature Imm. Empty n were calculated for the period 1982− 2010 using the NOAA Pathfinder A. aspera 75 25 0 4 dataset v5.2. SSTs for 2010 and 2012 A. bushyensis 075254 SSTs were calculated from the on-reef A. clathrata 7 87 7 15 100 0 0 5 sensor network of the Great Barrier A. muricata 46 0 54 26 Reef Ocean Observing System and A. gemmifera 0 100 0 1 A. glauca 0 80 20 10 61 0 39 64 the Australian In stitute of Marine Sci- A. horrida 25 0 75 8 ence (http://data. aims. gov.au/ gbroos/). A. humilis 0 0 100 5 Mean monthly PAR was calculated A. hyacinthus 100 0 0 2 0 0 100 1 for the period 1999−2010 using data A. latistella 100 0 0 2 from NASA (MODIS; http:// oceancolor. A. loripes 0 0 100 1 gsfc. nasa.gov/). Mean monthly rain- A. lovelli 67 33 0 3 45 0 55 11 fall and wind speed data were A. microphthalma 050506 A. nana 0 100 0 3 obtained for the period 1999−2010 A. nasuta 100 0 0 3 using data from NASA/NOAA (TMI, A. solitaryensis 0 100 0 5 0 0 100 1 www.remss. com/missions/ tmi). Acropora sp. nov. 1 0 0 100 2 0 0 100 2 Acropora sp. nov. 2 0 0 100 1 A. stoddarti 100 0 0 2 Species identifications A. tortuosa 0 100 0 2 A. valida 50 50 0 2 67 0 33 6 A. verweyi 33 0 67 3 Acropora spp. were identified in situ A. yongei 32 29 39 28 62 0 38 13 or from photographs or microscopic Total 18 58 24 83 54 1 45 158 examination of the skeleton following Wallace (1999). Species from other families were similarly identified following Veron (2000). The most recently accepted Coral spawning slicks were observed on 29 Decem- names for these species were then determined by a ber 2010 (Fig. 2a), 8 d after full moon. search at the World Register of Marine Species Between 12 and 14 January 2012, a total of 158 (www.marinespecies.org/ index.php). Many of the colonies were sampled from 18 species. Fifty-four corals on Lord Howe Island are highly distinctive and percent of colonies were mature, 45% were empty difficult to place within current morphological spe- and 1 colony was immature (Table 1). Twelve species cies boundaries. Indeed, there are likely to be a num- had at least 1 mature colony and 6 species were ber of undescribed species, including at least 4 we not gravid (Table 1). Coral spawning slicks were ob- examine here that will be described elsewhere. served on 19 January 2012 (Fig. 2b), 10 d after the full moon. Extensive field samples on 20 and 21 January 2012 found no Acropora colonies with mature oocytes. RESULTS

Stage of oocytes maturity of Acropora species Reproductive biology and spawning times of corals maintained in aquaria Between 12 and 14 December 2010, 83 colonies were sampled from 13 species (Table 1). Eighteen Of the 15 species collected for observation in the percent of colonies were mature, 58% were imma- laboratory, broadcast spawning was observed in 11 ture and 24% were empty. Four species had at least species and 1 species, Porites heronensis, released 1 mature colony and 11 species had colonies that planulae that were swimming when first observed at were immature (Table 1). Only 1 species was not 09:00 h in the morning (Table 2). Broadcast spawning gravid (i.e. neither mature nor immature oocytes was inferred to occur in Goniastrea favulus on the were detected) at the time of sampling (Table 1). basis of disappearance of mature oocytes from all 5 Baird et al.: Coral reproduction on Lord Howe Island 279 Max. egg een 24:00 and 06:00 h Symbiodinium y 2012, 9 to 13 d after the full moon

Fig. 2. Coral spawn slicks at Lord Howe Island: (a) North Bay, 29 December 2010, and (b) Main Beach, 19 December 2012 colonies at some point between initial collection of colonies on 13 January and a subsequent check of reproductive condition on 20 January 2012. We assumed these colonies spawned before 17:00 h when colonies were brought to the laboratory from storage under the jetty for observation. None of the 10 Acropora colonies spawned in the laboratory (Table 2); however, neither species had any oocytes in extensive sampling in the field on 20 January 2011. Of the species observed in the aquaria, 5 spawned on 19 January 2012, 10 d after the full moon, 6 on 20 January, and 3 on 21 January (Table 2). Acanthastrea hillae spawned in 2012 spawned spawning in bundles color in propagules diameter (µm) 30 min before sunset, Favites halicora and 1 colony of Platygyra daedalea spawned sometime between 00:00 and 06:00 h the next morning, and the remain- der of species spawned between 20:30 and 00:00 h (Table 2). Species observed to broadcast-spawn gametes were hermaphrodites (i.e. both eggs and sperm North BayNorth BayPot Holes 1North Bay 1North Bay 21 Jan 5Pot Holes 1 20 JanNorth Bay 1North Bay 19 Jan 5 naNorth Bay 1 1 19 JanHorseshoe 1 1 20 Jan 1 19 Jan 5 1 21:00 21 Jan 5 24:00+ 1 21 Jan 18 Jan 4 1 Yes 20:25 Yes 1 23:00 na 1 22:15 Orange Pink 1 Yes 23:30 24:00+ H Yes H 21:30 na Yes 24:00+ Red Yes Yes Red No Orange Planula No H Yes Red na Red H Brown Red H Brown na H No H G na No 352 352 No Yes No No No 308 308 na 374 na 352 352 462 were ap parent in gamete bundles), with the exception HorseshoePot HolesNorth Bay 5North Bay 1North Bay 1North Bay na 1 20 Jan 1 19 Jan 5 20 Jan 21 Jan 19 Jan 1 0 1 1 1 17:35 5 na 20:25 24:00 24:00 Yes Yes 21:10 na Yes Brown Yes Brown Yes H Red Red H Red Brown na H No H H No na No No No 484 440 352 na 286 352 of Goniopora norfolkensis, in which bundles contained only eggs. Egg diameters on release ranged from a minimum of 284 µm in the 2 Cyphastrea species to 484 µm in A. hillae (Table 2). Only P. heronensis had Symbiodinium spp. in its propagules (Table 2). sp. nov. North Bay 1 20 Jan 1 20:30 Yes Brown H No 286 sp. 3 nov. South Passage 5 na 0 na na Red na na na

Reproductive biology of species in the family Pocilloporidae Dipsastrea pallida Favites halicora Goniastrea favulus Hydnophora exesa Hydnophora exesa Paragoniastrea australensis Platygyra daedalea Platygyra daedalea Goniopora norfolkensis Porites heronensis Acropora glauca Acanthastrea hillae Echinophyllia aspera Astrea curta Astrea curta Cyphastrea microphthalma Cyphastrea Acropora

Oocytes were first observed in 3 out of 5 colonies of Seriatpora hystrix in October 2011. Two colonies had oocytes in November, 5 in December and January, on 9 January 2012. n: number of colonies collected; H: hermaphrodite; G: gonochore; na: no data; 24:00+: spawning occurred betw and 2 in February. Typically, there were only 1 or Family Species Site n Date spawned Colonies of Time Gametes Egg Sex Merulinidae Merulinidae Merulinidae Merulinidae Merulinidae Merulinidae Merulinidae Poritidae Poritidae Merulinidae Lobophyllidae Lobophyllidae Merulinidae Merulinidae Merulinidae Merulinidae Acroporidae Acroporidae

2 oocytes per polyp. Planulae were first observed in 2. ReproductiveTable biology of corals maintained in aquaria at the Lord Howe Island Research Station between 18 and 22 Januar 280 Aquat Biol 23: 275–284, 2015

2 colonies of S. hystrix in November 2011. Five on Lord Howe Island. Multi-specific synchronous colonies had planulae in December; 3, in January; spawning episodes occurred between dusk and mid- none, in February; and 2, in March. Typically, 1 plan- night, 8 to 12 d after full moons in December and ula was found in each polyp and very occasionally 2. January. Peak reproductive activity most probably Oocytes were first observed in all 5 colonies of Sty- occurs in January, because 24 species were either lophora pistillata in October 2011. All 5 colonies had observed or inferred to spawn over a 3 to 4 night oocytes in November; 3 in December; 2 in January period, 8 to 11 d after the full moon in January 2012 and none in February or March. Up to 9 oocytes were and 3 species also released planulae in January 2012. observed in a polyp. Planulae were first ob served in Spawning in December and January coincides with 3 out of 5 colonies of S. pistillata in November 2011. high and rising SST, high PAR, high rainfall and low Four colonies had planulae in December and 2 had wind speeds for the location. These spawning pat- them in January. Typically 1 or 2 planulae were terns are similar to most other locations in the Indo- found in each polyp, although up to 4 planulae were Pacific (Baird et al. 2009b). observed in a single polyp. No oocytes or planulae The proportion of Acropora spp. colonies and the were observed in Pocillopora damicornis. number of species inferred to spawn in January were similar in both years—58% of the colonies from 11 species in 2010 versus 54% of the colonies from 12 Gametogenic cycles and development of planulae species in 2012 (Table 1)—suggesting that this is the in pocilloporids typical pattern. The high proportion of colonies gravid (76%) in December 2010 suggests that repro- Samples for histology were first processed from ductive activity is unlikely to be strong in months colonies collected in October 2011 at which time, for other than December and January. Nonetheless, 5 of S. hystrix, both oocytes and spermaries were evident the 23 Acropora spp. sampled were not gravid. These in cross-section (Fig. 3a). Developing larvae were 5 species either breed at other times of the year, not first observed in November 2011, at which point at all, or, alternatively, not enough colonies were spermaries, oocytes and the developing larvae all co- sampled to detect gravid individuals. High reproduc- occur in the same branch (Fig. 3b). The largest tive output in December and January coincides with oocytes observed were approximately 140 µm (Fig. 3b). peaks in coral recruitment to settlement tiles placed Larvae were distinguished by their size (200 to 450 µm between December and March (Harriott 1992). in diameter in cross-section; Fig. 3b,c), deep red- The sexuality and mode of reproduction of each staining yolk cells and an epidermis (Fig. 3c,d). Plan- species are similar to previous records in the Indo- ulae were first observed in November and were Pacific (Baird et al. 2009b). Novel observations in- distinguished by a well-differentiated gastrodermis clude the first record of the mode of reproduction in and an epidermis with nematocysts and gland cells Acanthastrea hillae and Cyphastrea sp. nov., which (Fig. 3e,f). Planulae were approximately 450 to 550 µm are both broadcast spawners, and Porites heronensis, in cross-section (Fig. 3e,f). which is a brooder. P. heronensis is highly abundant in the lagoon at Lord Howe Island, and, together with other species known to brood on Lord Howe Island or Environmental conditions during spawning elsewhere (Seriatopora hystrix, Stylophora pistillata, Isopora cuneata, P. damicornis), makes up >60% Spawning at Lord Howe Island coincided with of the coral cover in the lagoon (Keith et al. 2015). rising SST and occurred prior to the historical peak The dominance of brooding species in coral assem- in SST of 24°C in March and April (Fig. 4a). Coral blages at Lord Howe Island was first noted by Har- spawning occurred when PAR was at a maximum riott (1992) who hypothesised that rapid settlement of (Fig. 4b), monthly rainfall was relatively high (Fig. 4c), brooded larvae allows these species to establish pop- and wind speeds were relatively low when compared ulations in isolated locations such as Lord Howe to other months (Fig. 4d). Island. An alternative hypothesis is that internal fertilization (i.e. brooding) is a more successful reproductive strategy than external fertilization (i.e. DISCUSSION broadcast spawning) in the sub-tropical waters of Lord Howe Island. In 2 species of broadcast spawn- Here, we documented the month or time of spawners, median larval lifespan was very low: <24 h for ing of more than half of the approximately 65 species both Paragoniastrea australensis and Cyphastrea Baird et al.: Coral reproduction on Lord Howe Island 281

Fig. 3. Gametogenic cycles and development of brooded planulae in Seriatopora hystrix at Lord Howe Island: (a) oocytes in polyps in October 2011; (b) oocytes, spermaries and developing larvae in polyps in November 2011; (c) developing larvae, distinguished by their size (~300 µm diameter), deep red-staining yolk cells, and epidermis, and spermaries in adjacent polyps in November 2011; (d) close-up of developing larvae showing epidermis; (e) larvae in polyps with developing mesenteries and epidermis in November 2011; and (f) fully developed planula larvae in a polyp in December 2011. o: oocytes; s: spermaries; l: developing larvae; p: planulae; m: mesenteries; e: epidermis; g: gastrodermis micro phthalma (Woolsey et al. 2014) compared to to the marginal environmental conditions experi- typical values of >30 d among the larvae of broad- enced in Lord Howe Island waters, such as winter cast-spawning species at tropical locations (Graham temperatures of 14.4°C (Woolsey et al. 2014). This et al. 2008, Connolly & Baird 2010). This suggests might have a detrimental effect on the development that gametes of these sub-tropical broadcast-spawning of gametes in broadcast-spawning species that have corals were either of poor quality or highly sensitive an oogenic cycle of between 6 and 14 months (Harri- to handling. Poor-quality larvae could be attributed son & Wallace 1990). In contrast, brooding species 282 Aquat Biol 23: 275–284, 2015

28 ab50

26 ) –1 s

24 –2 40

22 SST (°C) 30

20 (µE m PAR

18 20 0.13

cd) 9.0 –1

0.11 8.5

8.0 0.09 Rainfall (m)

Wind speed (km s 7.5 0.07

Jul Apr Jul Apr Aug Sep Oct Nov Dec Jan Feb Mar May Jun Aug Sep Oct Nov Dec Jan Feb Mar May Jun Fig. 4. Environmental variables hypothesised to be involved in synchronising coral spawning: (a) mean monthly sea-surface temperature (SST) for the period 1982−2010 (black line), 2010 (red line) and 2012 (blue line); (b) mean monthly photosyntheti- cally active radiation (PAR); (c) mean monthly rainfall; and (d) mean monthly wind speeds for the period 1999−2010 (data sources are listed in the ‘Materials and methods’ section). Spawning times are indicated by the grey shading in each panel have an oogenic cycle of approximately 1 mo, and year of sampling. Despite previous conjecture (see only breed in the warmer months of the year on Lord citations in van Woesik 1995), this is the first time no Howe Island. Low survivorship of broadcast-spawned reproductive activity has been detected in a sclerac- propagules is consistent with the low densities of tinian coral species in the absence of obvious stress. recruits to settlement tiles on the substratum at Lord This result is possibly a sampling artefact. If the time Howe Island when compared with settlement in to develop from oocyte to planulae is <1 mo then tropical locations (Harriott 1992). the monthly sampling could have missed the cycle. Oocytes and larvae were first observed in Seriato- Indeed, previous estimates of a 2 wk oogenic cycle pora hystrix and Stylophora pistillata in October and in P. damicornis in Okinawa indicate this is a possi- November, respectively, suggesting an oogenic cycle bility (Permata et al. 2000). Further work is required of approximately 1 mo in these 2 species. Dissections to establish whether or not P. damicornis is reproduc- suggested that oocytes were produced monthly and tively active at Lord Howe Island. co-occur in the same polyps with developing larvae The patterns of spawning within the coral assem- (Fig. 1b). Planulae are likely to be released shortly blage at Lord Howe Island indicate that patterns in after maturity, indicating most colonies will planulate marginal reef locations are similar to those in loca- every month over a period of 3 to 4 mo. The length of tions elsewhere in the Indo-Pacific. This suggests the reproductive season in these brooders at Lord that the selective processes that drive spawning syn- Howe Island is similar to that at Heron Island but chrony are the same as those found in other regions contrasts with the period at more tropical locations of the Indo-Pacific. The highly seasonal nature of where planulation occurs throughout the year (Fan & coral reproduction at Lord Howe Island and elsewhere Dai 1996, Tanner 1996). In contrast, no reproductive means that managing human activities to reduce the activity was observed in Pocillopora damicornis: threat from processes that affect reproductive suc- neither oocytes nor planulae were recorded in 300 cess, such as dredging, appears quite feasible once polyps from a possible 60 colonies over a complete the timing of these events is established. Baird et al.: Coral reproduction on Lord Howe Island 283

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Editorial responsibility: Judith Grassle, Submitted: November 26, 2014; Accepted: February 14, 2015 New Brunswick, New Jersey, USA Proofs received from author(s): April 2, 2015